Merriweather was drafted in the 3rd round (70th pick overall) of the 1982 NFL Draft by the Pittsburgh Steelers.[3] His first professional season was 1982 with the Steelers and he was elected to the Pro Bowl in three consecutive seasons: 1984, 1985, and 1986.[4] In 1984 he was 5th in the NFL with 15 sacks (Mark Gastineau led the league with 22), and was named first-team all-NFL that year.[5] He was named Pittsburgh Steelers' Most Valuable Player in 1987.[6]

After a salary dispute which saw him sit out the entire 1988 season, he was traded to the Minnesota Vikings for a first-round pick.[7] In 1989, his first season at Minnesota, he became the first player in NFL history to score the winning points in an overtime game with a safety[8] when he blocked a punt out of the end zone in a game against the Los Angeles Rams for a final score of 23-21, the same game in which the Vikings' Rich Karlis had scored a then-record 7 field goals to get the 21 points that sent the game into overtime.[9]

In 1993, Merriweather was inducted into the Pacific Athletics Hall of Fame.[12] He was inducted into the Vallejo Sports Hall of Fame in 2004,[13] and was inducted into the Sac-Joaquin Section Hall of Fame in 2012.[14]